Of possums and pit vipers: an evolutionary duel

September 12, 2011

Sharon Jansa, seen here with a non-snake-eating mouse opossum, is an associate professor in the Department of Ecology, Evolution and Behavior in the University of Minnesota's College of Biological Sciences and curator of mammals at the University's Bell Museum of Natural History.

A case study in how evolution works

By Deane Morrison

Whoever heard of a mild-mannered marsupial like the Virginia opossum eating rattlesnakes?

Rattlesnakes strike with lightning speed; yet certain opossums not only survive, but go on to eat the snakes. How do they do it?

In a new study, University of Minnesota researcher Sharon Jansa and colleague Robert Voss of the American Museum of Natural History show that rapid evolution of a blood protein keeps the Virginia opossum and related species one step ahead of evolutionary "upgrades" in the potency of the viper's venom.

Published in the journal PLoS ONE, the work injects a new element into the story of the perpetual "arms race" between predators and prey, in which each continually evolves new offenses or defenses to thwart the other's arsenal. It also lays bare the nuts and bolts of evolution, showing how, although invisible, rapid evolutionary changes in just one protein can make a big difference in what an animal eats and what predatory attacks it can survive.

It was already well known that pit viper venoms evolved quickly. Previously, evolutionary biologists seeking the explanation had looked at the blood proteins of prey animals like rodents. But they could find no evidence of rapid evolution among potential genes for venom resistance, and thus no force that could be driving the evolution of snake venom.

The work of Jansa and Voss produces the evidence and shows that the right place to look was not in the mammals and birds that snakes stalk, but in the unobtrusive opossums that stalk the snakes.

"It's not every day you get a ringside seat to watch evolution in action," says Jansa, the curator of mammals at the University's Bell Museum of Natural History. "We have here a nice case of co-evolution between a mammal and its potential prey.

"What's cool about it is the evolution of molecules. Snake venom evolves incredibly rapidly, and opossums are probably evolving in response."

The arsenals

Jansa and Voss began by studying the genomes of opossums, looking for similarities and differences among species that could help in constructing an evolutionary tree for them. They noticed that in the "tribe" of opossums that eats pit vipers—a group of venomous snakes that includes rattlesnakes—the gene for a certain blood protein was riddled with mutations.

But not just any mutations. There are two basic kinds of mutations. Some are silent; to visualize this, imagine a gene sequence as a radio script. Changing a script so that "two" becomes "to" or "too" won't change the meaning to a listener. Likewise, in genetics, some mutations in DNA are "silent substitutions," in which one DNA building block is substituted for another but the change has no effect on the amino acid composition of proteins.

In contrast, mutations called "replacement substitutions" not only alter the genetic instructions—like changing "two" to "twenty"—but also replace one amino acid with another; this can have a profound effect on the behavior of a protein.

In Jansa and Voss's case, the protein was von Willebrand factor, a key element in blood clotting and a target of rattlesnake venom. Among the snake-eating opossums, the gene for von Willebrand showed a high proportion of replacement substitutions compared to silent ones.

That doesn't mean the gene is mutating faster; mutations are largely random events. But when many replacement substitutions in a single gene have become the norm in a population, it's a sign that those mutations give their bearers an advantage.

"We think it's Darwinian, or positive, selection, which means the mutations increase the probability of survival," says Jansa. "In most molecules, silent substitutions far outpace replacement substitutions. What's unique about the snake eaters is that they have an elevated rate of replacement substitutions in the gene for von Willebrand factor. This is strong evidence for positive selection."

So it goes like this: A rattlesnake venom gene mutates and becomes more potent against von Willebrand factor. This means some former snake-eating opossums will lose their resistance and succumb to rattlesnakes. But thanks to the rapid mutation of opossum von Willebrand factor, others will have a new, resistant version of the factor and so will survive being bitten. They will keep on eating rattlesnakes, and the gene for the new von Willebrand factor will spread. This sort of back-and-forth is known as an evolutionary arms race.

It's about food

The evolution in opossum von Willebrand factor is essentially an adaptation that affects what the animals can eat.

'It's like the difference in dentition for eating meat vs. nectar vs. mollusks—the dentition is different for herbivores and carnivores," says Jansa. "But these opossums are generalists—they eat anything—so they don't have specialized dentitions. We seem to have found a molecular adaptation, instead of a dental adaptation, that enables them to expand their diet."